The hippocampus supports high-resolution binding in the service of perception, working memory and long-term memory

Abstract

It is well established that the hippocampus plays a critical role in our ability to recollect past events. A number of recent studies have indicated that the hippocampus may also play a critical role in working memory and perception, but these results have been highly controversial because other similar studies have failed to find evidence for hippocampal involvement. Thus, the precise role that the hippocampus plays in cognition is still debated. In the current paper, I propose that the hippocampus supports the generation and utilization of complex high-resolution bindings that link together the qualitative aspects that make up an event; these bindings are essential for recollection, and they can also contribute to performance across a variety of tasks including perception and working memory. An examination of the existing patient literature provides support for this proposal by showing that hippocampal damage leads to impairments on perception and working memory tasks that require complex high-resolution bindings. Conversely, hippocampal damage is much less likely to lead to impairments on tasks that require only low-resolution or simple associations/relations. The current proposal can be distinguished from earlier accounts of hippocampal function, and it generates a number of novel predictions that can be tested in future studies.

Keywords: Amnesia; Familiarity; Hippocampus; Recognition; Recollection.

Figure 1

Variations in the resolution and associative nature of binding. Each shape reflects a different item (e.g., word, object, odor), whereas color is used to represent a quality of that item (e.g., hue, location, pleasantness). Representations vary from low-resolution (e.g., orange vs blue, left vs right) to high-resolution (e.g., precise color, precise location), and from simple (e.g. object-color, object-object) to complex bindings (e.g., color-object-object-color). Complex high-resolution representations are expected to be the most hippocampally dependent (dark end of gradient), whereas simple low-resolution bindings will be the least hippocampally dependent (light end of gradient). The extent to which specific bindings will be dependent on the hippocampus or cortex varies across this gradient, and varies as a function of temporal delay inherent in various long-term memory (LTM), working memory (WM) and perception tasks.

Figure 2

(A) An illustration of the ‘same/different’ perceptual discrimination task. Individuals indicate their confidence that the scenes are the same or different. The two scenes are either identical or have been slightly altered. (B) Receiver operating characteristics for controls and patients with medial temporal lobe damage (left), along with estimates of state and strength-based perception in each group (right). Hippocampal damage reduced strength-based perception, but did not impact state-based perceptual responses (Aly, Ranganath, & Yonelinas, 2013).